Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T19:24:16.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Non-insulin-mediated glucose uptake in fed and fasted sheep

Published online by Cambridge University Press:  18 August 2016

T. E. C. Weekes ,
Y. Obara  and
M. T. Rose
T. E. C. Weekes*
Affiliation:
Department of Biological and Nutritional Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne NE1 7RU, UK
Y. Obara*
Affiliation:
National Institute of Animal Industry, Tsukuba Norindanchi, PO Box 5, Ibaraki 305 – 0901, Japan
M. T. Rose*
Affiliation:
National Institute of Animal Industry, Tsukuba Norindanchi, PO Box 5, Ibaraki 305 – 0901, Japan
*
†Present addresses: Corresponding author. Faculty of Agriculture, Tohoku University, Amamiya-matchi, Tsutsumi-dori, Aoba-ku, Sendai 981-8555, Japan.
‡Institute of Rural Studies, University of Wales, Aberystwyth SY23 3AL, UK.
‡Institute of Rural Studies, University of Wales, Aberystwyth SY23 3AL, UK.
Get access

Abstract

In ruminants and humans, the majority of whole body glucose utilization is not mediated by insulin. However, while in man most non-insulin-mediated glucose utilization (NIMGU) occurs in the brain, in ruminants the locations of NIMGU remain less well defined. As fasting would be expected to limit NIMGU to what would be regarded as an essential minimum, two studies were performed to establish the contribution of NIMGU to total glucose metabolism in fed and fasted sheep. Each study used four adult castrated male sheep. In study 1, a primed continuous infusion of U- [13C] glucose was begun at time 0 and continued for 7 h. After 3 h of isotope infusion (basal period) somatostatin (0•417 µg/kg per min; SS) was administered for 4 h, either alone (SS-only) or together with insulin (1•0 mU/kg per min; SS + insulin) with normal glucose to maintain euglycaemia for 2 h. Normal glucose was then infused for both the SS-only and SS + insulin treatments to induce and maintain hyperglycaemia over the final 2 h of the experiment. In study 2, fed or 72-h fasted sheep were infused with 6-[3H] glucose from time 0 for 8 h, with SS infusion starting at 3 h and continuing for 5 h. After 3 h of SS infusion, glucose was infused to induce and maintain hyperglycaemia. In both studies SS infusion inhibited insulin secretion, however in study 2, SS in fed sheep caused hyperglycaemia; this effect was not significant in the fasted animals. The rate of glucose utilization was reduced by SS-only as it eliminated insulin mediated glucose uptake (IMGU); under such conditions whole body glucose disposal should be NIMGU. In fed sheep, average NIMGU levels represented between proportionately 0•61 and 0•67 of the basal glucose metabolic clearance rate. During the infusion of SS + insulin in fed sheep, NIMGU fell to 0•34 during euglycaemia and 0•33 during hyperglycaemia, as the infused insulin caused IMGU to predominate. In fasted sheep the absolute rates of both IMGU and NIMGU were reduced, though NIMGU as a proportion of total turn-over (IMGU + NIMGU) increased to 0•88 of glucose metabolic clearance. Calculations suggest that, in contrast to man, only a minor proportion of NIMGU is utilized by the brain and central nervous system in fed or fasted sheep. It is suggested that skeletal muscle and the gastro-intestinal tract may make a major contribution to NIMGU, even in fasted sheep.

Keywords

fastingglucoseinsulinsheep
Type
Research Article
Information
Animal Science , Volume 71 , Issue 3 , December 2000 , pp. 453 - 463
Copyright
Copyright © British Society of Animal Science 2000

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Balcells, J., Seal, C. J. and Parker, D. S. 1995. Effect of intravenous glucose infusion on metabolism of portal-drained viscera in sheep fed a cereal/straw-based diet. Journal of Animal Science 73: 2146—2155.CrossRefGoogle ScholarPubMed
Baron, A. D., Brechtel, G., Wallace, P. and Edelman, S. V. 1988a. Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. American Journal of Physiology 255: E769—E774.Google ScholarPubMed
Baron, A. D., Brechtel, G., Wallace, P. and Edelman, S. V. 1988b. Fasting decreases rates of non-insulin-mediated glucose uptake in man. Journal of Clinical Endocrinology and Metabolism 67: 532—540.CrossRefGoogle Scholar
Baron, A. D., Kolterman, O. G., Bell, J., Mandarino, L. J. and Olefsky, J. M. 1985. Rates of non-insulin- mediated glucose uptake are elevated in type II diabetic subjects. Journal of Clinical Investigation 76: 1782—1788.CrossRefGoogle Scholar
Bergman, E. N. 1975. Production and utilization of metabolites by the alimentary tract as measured in portal and hepatic blood. In Digestion and metabolism in the ruminant (ed. McDonald, I. W. and Warner, A. C. I.), pp. 292—305. University of New England Publishing Unit, Armidale, USA.Google Scholar
Bergman, R. N., Ader, M., Finegood, D. T. and Pacini, G. 1984. Extrapancreatic effect of somatostatin infusion to increase glucose clearance. American Journal of Physiology 247: E370—E379.Google ScholarPubMed
Best, J. D., Taborsky, G. J., Halter, J. B. and Porte, D. 1981. Glucose disposal is not proportional to plasma glucose level in man. Diabetes 30: 847—850.CrossRefGoogle Scholar
Cowan, J. S. and Hetenyi, G. 1971. Glucoregulatory responses in normal and diabetic dogs recorded by a new tracer method. Metabolism 20: 360—372.CrossRefGoogle ScholarPubMed
Fell, B. F., Campbell, R. M., Mackie, W. S. and Weekes, T. E. C. 1972. Changes associated with pregnancy and lactation in some extra-reproductive organs of the ewe. Journal of Agricultural Science, Cambridge 79: 397—407.CrossRefGoogle Scholar
Fuller, M. F., Weekes, T. E. C., Cadenhead, A. and Bruce, J. B. 1977. The protein-sparing effect of carbohydrate. 2. The role of insulin. British Journal of Nutrition 38: 489—496.CrossRefGoogle ScholarPubMed
Gross, K. L., Harmon, D. L., Minton, J. E. and Avery, T. B. 1990. Effects of isoenergetic infusions of propionate and glucose on portal-drained visceral nutrient flux and concentrations of hormones in lambs maintained by total intragastric infusion. Journal of Animal Science 68: 2566—2574.CrossRefGoogle ScholarPubMed
Hocquette, J. F., Bornes, F., Balage, M., Ferre, P. , Grizard, P. and Vermorel, M. 1995. Glucose-transporter (GLUT 4) protein content in oxidative and glycolytic muscles from calf and goat. Biochemical Journal 305: 465—470.CrossRefGoogle ScholarPubMed
Janes, A. N., Weekes, T. E. C. and Armstrong, D. G. 1985. Insulin action and glucose metabolism in sheep fed on dried-grass or ground, maize-based diets. British Journal of Nutrition 54: 459—471.CrossRefGoogle ScholarPubMed
Johke, T. 1978. Effects of TRH on circulating growth hormone, prolactin and triiodothyronine levels in the bovine. Endocrinologica Japonica 25: 19—26.CrossRefGoogle ScholarPubMed
Laarveld, B., Christensen, D. A. and Brockman, R. P. 1981. The effect of insulin on net metabolism of glucose, amino acids by the bovine mammary gland. Endocrinology 108: 2217—2221.CrossRefGoogle ScholarPubMed
Lang, C. H. 1992. Rates and tissue sites of noninsulin- and insulin-mediated glucose uptake in diabetic rats. Proceedings of the Society for Experimental Biology and Medicine 199: 81—87.CrossRefGoogle ScholarPubMed
Lavelle-Jones, M., Scott, M. H., Kolterman, O., Moosa, A. R. and Olefsky, J. M. 1987. Non-insulin-mediated glucose predominates in postabsorptive dogs. American Journal of Physiology 252: E660—E666.Google ScholarPubMed
Lindsay, D. B. and Setchell, B. P. 1976. The oxidation of glucose, ketone bodies and acetate by the brain of normal and ketonaemic sheep. Journal of Physiology 259: 801—823.CrossRefGoogle ScholarPubMed
Metcalf, J. A. and Weekes, T. E. C. 1990. Effect of plane of nutrition on insulin sensitivity during lactation in the ewe. Journal of Dairy Research 57: 465—478.CrossRefGoogle ScholarPubMed
Okine, E. K., Glimm, D. R., Thompson, J. R. and Kennelly, J. J. 1995. Influence of stage of lactation on glucose and glutamine metabolism in isolated enterocytes from dairy cattle. Metabolism 44: 325—331.CrossRefGoogle ScholarPubMed
Pell, J. M. and Bergman, E. N. 1983. Cerebral metabolism of amino acids and glucose in fed and fasted sheep. American Journal of Physiology 244: E282—289.Google ScholarPubMed
Pethick, D. W. 1993. Carbohydrate and lipid oxidation during exercise. Australian Journal of Agricultural Research 44: 431—441.CrossRefGoogle Scholar
Pethick, D. W., Lindsay, D. B., Barker, P. J. and Northrop, A. J. 1981. Acetate supply and utilisation by the tissues of sheep in vivo . British Journal of Nutrition 46: 97—110.CrossRefGoogle ScholarPubMed
Rose, M. T. and Obara, Y. 1996. Effect of growth hormone on the response to insulin and glucose turnover in sheep. Journal of Agricultural Science, Cambridge 126: 107—115.CrossRefGoogle Scholar
Rose, M. T., Obara, Y., Itoh, F., Hashimoto, H. and Takahashi, Y. 1997a. Growth hormone does not affect non-insulin-mediated glucose uptake in sheep. Experimental Physiology 82: 749—760.CrossRefGoogle Scholar
Rose, M. T., Obara, Y., Itoh, F., Hashimoto, H. and Takahashi, Y. 1997b. Non-insulin-and insulin-mediated glucose uptake in dairy cows. Journal of Dairy Research 64: 341—353.CrossRefGoogle ScholarPubMed
Sano, H., Fujita, T., Okoshi, Y., Sasaki, M., Tsushida, M., Hara, S., Tomizawa, N. and Ambo, K. 1997. Effect of mild cold exposure on whole-body and net hindquaters glucose metabolism in sheep. Comparative Biochemistry and Physiology 116B: 95—98.CrossRefGoogle Scholar
Steele, R., Wall, J. S., De Bodo, R. C. and Altszuler, N. 1956. Measurement of size and turnover rate of body glucose pool by the isotope dilution method. American Journal of Physiology 187: 15—24.CrossRefGoogle ScholarPubMed
Weekes, T. E. C. 1991. Hormonal control of glucose metabolism. In Physiological aspects of digestion and metabolism in ruminants (ed. Tsuda, T., Sasaki, Y. and Kawashima, R.), pp. 183—200. Academic Press, San Diego, USA.CrossRefGoogle Scholar
Weekes, T. E. C. 1992. Influence of experimental hyperthyroidism on insulin action in growing sheep. Metabolism 41: 246—252.CrossRefGoogle ScholarPubMed
Weekes, T. E. C., Sasaki, Y. and Tsuda, T. 1983. Enhanced responsiveness to insulin in sheep exposed to cold. American Journal of Physiology 244: E335—E345.Google ScholarPubMed